No Laughing Matter: Intranasal Oxytocin Administration Changes Functional Brain Connectivity during Exposure to Infant Laughter
Open accessAbstract
Infant laughter is a rewarding experience. It activates neural reward circuits and promotes parental proximity and care, thus facilitating parent-infant attachment. The neuropeptide oxytocin might enhance the incentive salience of infant laughter by modulating neural circuits related to the perception of infant cues. In a randomized controlled trial with functional magnetic resonance imaging we investigated the influence of intranasally administered oxytocin on functional brain connectivity in response to infant laughter. Blood oxygenation level-dependent responses to infant laughter were measured in 22 nulliparous women who were administered oxytocin and 20 nulliparous women who were administered a placebo. Elevated oxytocin levels reduced activation in the amygdala during infant laughter and enhanced functional connectivity between the amygdala and the orbitofrontal cortex, the anterior cingulate, the hippocampus, the precuneus, the supramarginal gyri, and the middle temporal gyrus. Increased functional connectivity between the amygdala and regions involved in emotion regulation may reduce negative emotional arousal while enhancing the incentive salience of the infant laughter.
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Other studies have reported that oxytocin effects on amygdala responses often occur with concurrent changes in its connections with, and activation of, the insula.
“Indeed, other studies have also reported that OXT effects on amygdala responses often occur with concurrent changes in its connections with, and activation of, the insula (27 -29).”
From Oxytocin, the peptide that bonds the sexes also divides them (2016) · cites this paper as [29]
Only a few studies have examined the effects of OXT on functional connectivity in humans.
“To date, only a few studies have examined the effects of OXT on functional connectivity in humans (Dodhia et al, 2014;Domes et al, 2007;Riem et al, 2012;Sripada et al, 2013).”
From Oxytocin modulation of amygdala functional connectivity to fearful faces in generalized social anxiety disorder (2015) · cites this paper as Riem et al, 2012
OFC activation may reflect an augmented salience of social contact.
“It thus appears that OFC activation may reflect an augmented salience of social contact”
From An oxytocin-induced facilitation of neural and emotional responses to social touch correlates inversely with autism traits (2014) · cites this paper as Riem et al, 2012
While hearing infant's laughter, IN-OT reduces activation of amygdala and enhances functional connectivity between amygdala and OFC, ACC, hippocampus, and precuneus.
“While hearing infant’s laughter, IN-OT reduces the activation of the amygdala and enhances the functional connectivity between the amygdala and the OFC, ACC, hippocampus, and precuneus (Riem et al. 2012).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Riem et al. 2012
Connectivity within this neural network can be enhanced by intranasal oxytocin.
“Consistent with other studies (Bos et al., 2012) a previous study showed that connectivity within this neural network can be enhanced by intranasal oxytocin (Riem et al., 2012), which in turn facilitates the integration of emotion and cognition and the evaluation of emotional signals (Pessoa, 2008).”
From Oxytocin effects on complex brain networks are moderated by experiences of maternal love withdrawal (2013) · cites this paper as Riem et al., 2012
Oxytocin increased connectivity between the amygdala and the PCC and other emotional brain regions during exposure to infant laughter.
“in which we found that oxytocin increased connectivity between the amygdala and the PCC and other emotional brain regions during exposure to infant laughter (Riem et al., 2012).”
From Oxytocin effects on complex brain networks are moderated by experiences of maternal love withdrawal (2013) · cites this paper as Riem et al., 2012
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Gao, S., Becker, B., Luo, L., Geng, Y., Zhao, W., Yin, Y., Hu, J., Gao, Z., Gong, Q., Hurlemann, R., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1602620113 · Cited by 186 · see citing works
Freeman, S. M., Inoue, K., Smith, A. L., Goodman, M. M., & Young, L. J. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.03.023 · Cited by 185 · see citing works
“In humans, IN-OT affects the reaction to infant cries (Bakermans-Kranenburg et al., 2012) and infant laughter (Riem et al., 2012) and may even play a role in navigating the ‘‘cocktail party effect’’ (Tops et al., 2011), which is the phenomenon whereby an individual can focus one’s auditory…”
BackgroundIntranasal oxytocin attenuates the cortisol response to physical stress: a dose-response study
Cardoso, C., Ellenbogen, M. A., Orlando, M. A., Bacon, S. L., & Joober, R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.07.013 · Cited by 187 · see citing works
Johnson, Z. V., Walum, H., Jamal, Y. A., Xiao, Y., Keebaugh, A. C., Inoue, K., & Young, L. J. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.11.011 · Cited by 190 · see citing works
MacDonald, K., & Feifel, D. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00035 · Cited by 181 · see citing works
Wigton, R., Radua, J., Allen, P., Averbeck, B., Meyer-Lindenberg, A., McGuire, P., Shergill, S. S., & Fusar-Poli, P. (2015) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.130289 · Cited by 179 · see citing works
Intranasal administration of oxytocin: behavioral and clinical effects, a review
Veening, J. G., & Olivier, B. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.04.012 · Cited by 169 · see citing works
Scheele, D., Kendrick, K. M., Khouri, C., Kretzer, E., Schläpfer, T. E., Stoffel-Wagner, B., Güntürkün, O., Maier, W., & Hurlemann, R. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.78 · Cited by 171 · see citing works
Yamasue, H., Yee, J. R., Hurlemann, R., Rilling, J. K., Chen, F. S., Meyer-Lindenberg, A., & Tost, H. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3327-12.2012 · Cited by 149 · see citing works
Oxytocin׳s role in anxiety: A critical appraisal
MacDonald, K., & Feifel, D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.025 · Cited by 139 · see citing works
Elevated salivary levels of oxytocin persist more than 7 h after intranasal administration
van IJzendoorn, M. H., Bhandari, R., van der Veen, R., Grewen, K. M., & Bakermans-Kranenburg, M. J. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00174 · Cited by 137 · see citing works
Self-citationDissecting the Role of Oxytocin in the Formation and Loss of Social Relationships
Hurlemann, R., & Scheele, D. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.05.013 · Cited by 136 · see citing works
Riem, M. M. E., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Out, D., & Rombouts, S. A. R. B. (2012) · Attachment & Human Development · doi:10.1080/14616734.2012.727252 · Cited by 134 · see citing works
Self-citationGorka, S. M., Fitzgerald, D. A., Labuschagne, I., Hosanagar, A., Wood, A. G., Nathan, P. J., & Phan, K. L. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.168 · Cited by 131 · see citing works
Ma, Y., Shamay-Tsoory, S., Han, S., & Zink, C. F. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.10.009 · Cited by 131 · see citing works
Koch, S. B. J., van Zuiden, M., Nawijn, L., Frijling, J. L., Veltman, D. J., & Olff, M. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.11.018 · Cited by 123 · see citing works
Grace, S. A., Rossell, S. L., Heinrichs, M., Kordsachia, C., & Labuschagne, I. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.05.031 · Cited by 120 · see citing works
Oxytocin and the social brain: Neural mechanisms and perspectives in human research
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Hormonal contraceptives suppress oxytocin-induced brain reward responses to the partner’s face
Scheele, D., Plota, J., Stoffel-Wagner, B., Maier, W., & Hurlemann, R. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv157 · Cited by 116 · see citing works
“Specifically, it has been shown that OXT increased the arousal induced by infant photos in nulliparous women (Rupp et al., 2013) and promoted responsiveness to infant crying and laughter by reducing activation in anxiety-related neural circuits (Riem et al., 2011, 2012).”
BackgroundOxytocin receptors modulate a social salience neural network in male prairie voles
Johnson, Z. V., Walum, H., Xiao, Y., Riefkohl, P. C., & Young, L. J. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.10.009 · Cited by 113 · see citing works
Intranasal oxytocin enhances intrinsic corticostriatal functional connectivity in women
Bethlehem, R. A. I., Lombardo, M. V., Lai, M.-C., Auyeung, B., Crockford, S. K., Deakin, J., Soubramanian, S., Sule, A., Kundu, P., Voon, V, et al. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.72 · Cited by 96 · see citing works
“For example, previous studies examining functional connectivity during tasks show enhanced connectivity in women but decreased connectivity in men (Riem et al., 2012; Wittfoth-Schardt et al., 2012).”
Oxytocin effects on complex brain networks are moderated by experiences of maternal love withdrawal
Riem, M. M. E., van IJzendoorn, M. H., Tops, M., Boksem, M. A. S., Rombouts, S. A. R. B., & Bakermans-Kranenburg, M. J. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.01.011 · Cited by 91 · see citing works
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Frijling, J. L., van Zuiden, M., Koch, S. B. J., Nawijn, L., Veltman, D. J., & Olff, M. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.278 · Cited by 60 · see citing works
Circuits for social learning: a unified model and application to autism spectrum disorder
DeMayo, M. M., Young, L. J., Hickie, I. B., Song, Y. J. C., & Guastella, A. J. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.034 · Cited by 52 · see citing works
An integrated framework for the role of oxytocin in multistage social decision‐making
Piva, M., & Chang, S. W. C. (2018) · American Journal of Primatology · doi:10.1002/ajp.22735 · Cited by 38 · see citing works
“…as a line of research ultimately including a sample size of over 300 participants determined that OT increases activation in the ventral striatum inmen but decreases activation in the same region in women during the canonical prisoner's dilemma game (Feng et al., 2015; Rilling et al., 2012, 2014).”
BackgroundA precision medicine approach to oxytocin trials
Andari, E., Hurlemann, R., & Young, L. J. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_29 · Cited by 40 · see citing works
Intranasal oxytocin modulates neural functional connectivity during human social interaction
Rilling, J. K., Chen, X., Chen, X., & Haroon, E. (2018) · American Journal of Primatology · doi:10.1002/ajp.22740 · Cited by 40 · see citing works
Bhandari, R., Bakermans-Kranenburg, M. J., van der Veen, R., Parsons, C. E., Young, K. S., Grewen, K. M., Stein, A., Kringelbach, M. L., & van IJzendoorn, M. H. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.04.028 · Cited by 33 · see citing works
Self-citation
- Authors
- Riem, M. M. E., van IJzendoorn, M. H., Tops, M., Boksem, M. A. S., Rombouts, S. A. R. B., & Bakermans-Kranenburg, M. J.
- Affiliations
- Leiden University (NL)
- Radboud University Nijmegen (NL)
- Venue
- Neuropsychopharmacology
- Published
- 2011-12-21
- Volume
- 37
- Issue
- 5
- Pages
- 1257-1266
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC3306887
- OpenAlex
- W2124725885
- Cited by
- 191
- References
- 87
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 6 · 2023: 6 · 2022: 11 · 2021: 10 · 2020: 16 · 2019: 12 · 2018: 16 · 2017: 16 · 2016: 18 · 2015: 24 · 2014: 13 · 2013: 21 · 2012: 12
- FWCI
- 20.08
- Type
- journal article
- Language
- en
- Update notices
- erratum (2012-07-16)
- Open access
- bronze
- doi.org
- Locations
- Neuropsychopharmacology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion, other-oa)
- VU Research Portal (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Health Sciences › Health Professions › Pharmacy › Infant Health and Development
- Social Sciences › Psychology › Social Psychology › Humor Studies and Applications
- Keywords
- oxytocin, infant laughter, brain functional connectivity, amygdala, reward processing, incentive salience, parent-infant attachment, emotion regulation, nulliparous women, intranasal administration
- MeSH terms
- Acoustic Stimulation, Administration, Intranasal, Adult, Brain, Brain Mapping, Double-Blind Method, Female, Humans, Image Processing, Computer-Assisted, Infant, Laughter, Magnetic Resonance Imaging, Middle Aged, Oxygen, Oxytocics, Oxytocin, Reward, Twin Studies as Topic, Young Adult
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